Microorganisms consume trace gases present throughout the Mariana Trench water column

Abstract

Dark waters harbour two-thirds of the ocean's bacterial and archaeal cells, yet the energy sources sustaining microbial life at these depths remain poorly understood. Here we integrate hydrographic profiles with metagenomic analyses and ex situ activity measurements to investigate whether carbon monoxide (CO) and molecular hydrogen (H2) are viable energy sources for epipelagic and mesopelagic microbial populations in the Mariana Trench region. Both gases were detected from 5 to 9,371 m, with concentrations generally higher in the photic zone but anomalously high in several deeper waters. Metagenomic analyses indicate a shift from phototrophic towards lithotrophic energy acquisition with depth. Microbial populations encoding CO dehydrogenases increased from 6.1% at 5 m to 45% at 1,000 m, while those encoding uptake hydrogenases were much less abundant, but increased from 0.34% to 0.63%. Ex situ incubations revealed that in situ cell-specific CO oxidation rates declined with depth, whereas corresponding H2 oxidation rates were significantly higher at 1,000 m than at the surface. At 1,000 m, cell-specific H2 oxidation rates were approximately 4,500-fold higher than those of CO. These contrasting trends suggest that CO oxidation is a widespread auxiliary energy-acquisition strategy, whereas H2 oxidation may sustain hydrogenotrophic growth in dark waters. Together, our results suggest H2 and CO are readily available to pelagic microbial populations and are biologically oxidised in the dark zone, supporting microbial energy acquisition and oceanic biogeochemical cycling.